Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis-induced tumour formation

Mol Microbiol. 2011 Aug;81(3):751-66. doi: 10.1111/j.1365-2958.2011.07728.x. Epub 2011 Jun 22.

Abstract

Ustilago maydis is a biotrophic fungal pathogen that colonizes living tissue of its host plant maize. Based on transcriptional upregulation during biotrophic development we identified the pit (proteins important for tumours) cluster, a novel gene cluster comprising four genes of which two are predicted to encode secreted effectors. Disruption of the gene cluster abolishes U. maydis-induced tumour formation and this phenotype can be caused by deleting either pit1 encoding a transmembrane protein or pit2 encoding a secreted protein. Pit1 localizes to the fungal plasma membrane at hyphal tips, endosomes and vacuoles while Pit2 is secreted to the biotrophic interface. Both Δpit1 and Δpit2 mutants are able to penetrate maize epidermis and grow intracellularly at sites of infection but fail to spread in the infected leaf. Microarray analysis shows an indistinguishable response of the plant to infection by Δpit1 and Δpit2 mutant strains. Transcriptional activation of maize defence genes in infections with Δpit1/2 mutant strains indicates that the mutants have a defect in suppressing plant immune responses. Our results suggest that the activity of Pit1 and Pit2 during tumour formation might be functionally linked and we discuss possibilities for a putative functional connection of the two proteins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Membrane / chemistry
  • Endosomes / chemistry
  • Fungal Proteins / genetics
  • Fungal Proteins / metabolism*
  • Gene Deletion
  • Gene Expression Profiling
  • Genes, Fungal
  • Hyphae / chemistry
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism*
  • Multigene Family
  • Mutagenesis, Insertional
  • Plant Diseases / immunology
  • Plant Diseases / microbiology*
  • Plant Proteins / biosynthesis
  • Ustilago / pathogenicity*
  • Vacuoles / chemistry
  • Virulence Factors / genetics
  • Virulence Factors / metabolism*
  • Zea mays / immunology
  • Zea mays / microbiology*

Substances

  • Fungal Proteins
  • Membrane Transport Proteins
  • Plant Proteins
  • Virulence Factors